Insights into the cell-wall dynamics in grapevine berries during ripening and in response to biotic and abiotic stresses

Abstract

The cell wall (CW) is the dynamic structure of a plant cell, acting as a barrier against biotic and abiotic stresses. In grape berries, the modifications of pulp and skin CW during softening ensure flexibility during cell expansion and determine the final berry texture. In addition, the CW of grape berry skin is of fundamental importance for winemaking, controlling secondary metabolite extractability. Grapevine varieties with contrasting CW characteristics generally respond differently to biotic and abiotic stresses. In the context of climate change, it is important to investigate the CW dynamics occurring upon different stresses, to define new adaptation strategies. This review summarizes the molecular mechanisms underlying CW modifications during grapevine berry fruit ripening, plant-pathogen interaction, or in response to environmental stresses, also considering the most recently published transcriptomic data. Furthermore, perspectives of new biotechnological approaches aiming at modifying the CW properties based on other crops' examples are also presented.

Keywords: Botrytis cinerea; Berry development; Cell wall; Drought; Grapevine; Texture.

Fig. 1

Overview of Cell Wall Integrity (CWI) maintenance system to keep the functional integrity of the CW upon biotic (right side) and abiotic (left side) stresses. The main adaptive responses implemented by the plant upon recognition of DAMPs (red triangles) and PAMPs (blue circles) by plasma membrane receptors are indicated. During this process, changes in calcium (Ca²⁺) and reactive oxygen species (ROS) levels, mainly H₂O₂, occur. DAMPs (Damage-Associated Molecular Patterns), PAMPs (Pathogen-Associated Molecular Patterns), and CWMEs (Cell Wall Modifying Enzymes). The artwork was created using BioRender.com

Fig. 2

Schematic representation of CW modifications during berry development with the most modulated CWME-encoding gene members. Data refers to a transcriptional study on ‘Pinot Noir’ cultivar (Fasoli et al. 2018). For the abbreviations of the CWMEs, refer to Table 1. Red triangles: up-regulation; green triangles: down-regulation. The artwork was created using BioRender.com

Fig. 3

Expression heatmap of the eight most important classes of grapevine CWME-encoding genes showing the most interesting profile in 12 contrasts of the grapevine gene expression compendium VESPUCCI (Moretto et al. 2022). The heatmap visualizes the most significant results of those obtained and visualized in Online Resource 2. Each column of the heatmap corresponds to a contrast comparing B. cinerea infected vs. control samples. The accession numbers of the experiments retrieved by GEO (http://www.ncbi.nlm.nih.gov/geo/) and SRA (https://www.ncbi.nlm.nih.gov/sra) are the following: (1) GSE52586; (2) PRJNA414966; (3) GSE65969; (4) PRJNA281236. The color scale indicates the log2 expression ratio of each test (infected sample) vs. the reference condition (control sample) within each experiment. The genes are considered significantly differentially expressed if they fulfill a p-value of < 0.01 and an absolute log2 Fold Change (FC) value ≥ 1.0). E–L = Modified E–L (Eichhorn and Lorenz) system for grapevine growth stages from (Coombe 1995 ). For the abbreviations of the CWMEs refer to Table 1 . The heatmap was created using RStudio (ver 2023.09.1 + 494, R ver 4.3.2)

Fig. 4

Expression heatmap of the eight most important classes of grapevine CWME-encoding genes showing the most interesting profile in 30 contrasts of the grapevine gene expression compendium VESPUCCI (Moretto et al. 2022). The heatmap visualizes the most significant results of those obtained and visualized in Online Resource 3. Each column of the heatmap corresponds to a contrast comparing water-stressed vs. non-water-stressed conditions in leaf, root, and berry. The accession numbers of the experiments retrieved by GEO (https://www.ncbi.nlm.nih.gov/geo/) and SRA (https://www.ncbi.nlm.nih.gov/sra) are the following: (1) GSE57669; (2) GSE70670; (3) GSE126052; (4) GSE89075; (5) GSE89185; (6) GSE66391; (7) GSE72421. The color scale indicates the log2 expression ratio of each test (water-stressed sample) vs. the reference condition (control sample) within each experiment. The genes are considered significantly differentially expressed if they fulfill ap-value of < 0.01 and an absolute log2 Fold Change (FC) value ≥ 1.0). Water limitation conditions differ among the selected experiments. DAS = days after the beginning of stress application. For the abbreviation of the eight gene families, refer to Table 1 . The heatmap was created using RStudio (ver 2023.09.1 + 494, R ver 4.3.2)

Fig. 5

Schematic representation of the main CWME-encoding genes putatively involved in the berry-compatible interaction with Bc, both at early and late stages of infection, and under water stress conditions. The upper part of the figure focuses on the gene members most modulated during Bc infection in the susceptible wine cultivars ‘Marselan’ (at 48 hpi) (Kelloniemi et al. 2015) and ‘Pinot noir’ (at 12 wpi) (Haile et al. 2020). The lower part of the figure indicates the genes modulated under water stress conditions and shared by different organs: leaves (Catacchio et al. 2019), berries (Dal Santo et al. 2016) and roots (Yıldırım et al. 2018). Red triangles: up-regulation; green triangles: down-regulation. The artwork was created using BioRender.com